Journal of Mammalogy, 88(6):1447–1465, 2007
VOCAL STEREOTYPY AND SINGING BEHAVIOR IN BAIOMYINE MICE
JACQUELINE R. MILLER* AND MARK D. ENGSTROM Department of Natural History, Royal Ontario Museum, 100 Queens Park, Toronto, Ontario M5S 2C6, Canada (JRM, MDE) Department of Ecology and Evolutionary Biology, 25 Willcocks Street, Toronto, Ontario M5S 3B2, Canada (MDE, JRM)
We examined spectral features that characterize the highly stereotyped, repetitive vocalizations of New World baiomyine rodents. Although stereotyped vocal signaling, described as ‘‘song,’’ has been documented in Scotinomys (singing or brown mice), its occurrence was unknown in the sister taxon Baiomys (pygmy mice). We also recorded vocalizations of females, about which little information was previously available. Although examination of morphological and molecular data supports a close relationship between the 2 baiomyine genera, we identified song as a complex behavior that further underpins the monophyly of the Baiomyini. Both spectral and temporal features render these songs highly localizable, a characteristic of possible utility for courtship and other social behavior. The song of Baiomys is confined entirely to the ultrasonic spectrum, unlike that of Scotinomys, which uses a broader range of frequencies. The intensity, identity, and predictability of vocalization suggest that these songs are purposeful and carry information important for species identification.
Key words: Baiomyini, Baiomys, rodents, Scotinomys, song, stereotypy, ultrasound, vocal behavior
‘‘Nothing would work in the absence of communication.’’ within calls and songs (Catchpole and Slater 1995; Clark and (Hauser 1997) Wrangham 1993; Gil and Slater 2000; Hohmann and Fruth Animals communicate diverse information using vocal sig- 1994; Lengagne et al. 2001; Mitani et al. 1992; Mitani and nals, including identity, status, breeding condition, affective Marler 1989; Podos et al. 1992; Sloan et al. 2005; Zuberbu¨hler state, the likelihood of performing certain actions, and the char- 2002). These elements can be modified or reorganized to con- acteristics of environmental referents. These signals include vey a different message (e.g., Ackers and Slovodchidkoff 1999; loud ‘‘long calls’’ in mammals, which often encode information Win et al. 1981), or alter song attractiveness (see Catchpole and pertaining to territorial advertisement (e.g., Dempster et al. Slater [1995] for a review). 1992; Eisenberg and Lockhart 1972; Harrington 1983; The ability to locate conspecifics and maintain contact is Harrington and Mech 1979, 1983). Often stereotyped in either advantageous in territorial marking and reproductive behav- their form or in the manner of their repetition, these calls vary ior, as well as during social separation (Branchi et al. 2004; in complexity between taxa and in some species have been Hashimoto et al. 2001; Sales and Pye 1974). For animals that described as ‘‘song.’’ range broadly, or where maintaining social contact is difficult Songs are distinguished by how they are used, ‘‘being most when line of sight is lost, vocal signals can acquire charac- commonly given in the context of competition for resources teristics useful for both propagation and localization. Acous- (mates or food)’’ (Hauser 1997:95; see also Horn [1992] and tically, the ability to localize is facilitated by a number of Kroodsma [1982]). Songs also are distinguished from calls in mechanisms, such as when vocal signals are stereotypic (i.e., terms of structure and function, with songs tending to be longer signals that vary little in acoustic character or, if composed of in duration and more complex. In their entirety, they provide multiple elements, in chain structure), broadband or frequency taxonomic information and are useful tools to identify species modulated, repetitive, or ongoing (Lewis 1983; Sloan et al. and populations (Date et al. 1991; Geissman 1993; George 2005; Terhune 1974). The addition of temporal elements, such 1981; Haimoff et al. 1982; Thorpe 1961). A variety of studies as discrete terminal trailers, also can provide localizing cues also have identified distinct elements of meaning or syntax (Sloan et al. 2005). In alarm communication, the use of localizable calls can be advantageous if their emission allows the position of a threat to be monitored by distant conspecifics * Correspondent: [email protected] (Sloan et al. 2005). Yet localization increases the risk of predation for organisms that use such signals on a routine basis. Ó 2007 American Society of Mammalogists Moreover, high levels of stereotypy are likely expensive and www.mammalogy.org difficult to achieve for the sender (Eberhardt 1994; McCarty 1447 1448 JOURNAL OF MAMMALOGY Vol. 88, No. 6
Hafner 1978; Hooper and Carleton 1976; Packard 1960; Reid 1997; Sales and Pye 1974; this study). Some species are characterized by ecological or social conditions for which the ability to localize would be an asset (for instance, arboreal and monogamous mice). Few detailed acoustic analyses have been conducted on neotomines, or have they been presented in a phylogenetic context. This paper is part of an investigation of vocal behavior among the major lineages that constitute the Neotominae, with an emphasis on vocal stereotypy in taxa traditionally considered as peromyscines (Peromyscus and allied genera). The most spectacular of these signals are made by Scotinomys, a member of the tribe Baiomyini. Our focus is on vocal behavior in this tribe. The tribe Biaomyini includes 2 genera, Baiomys (pygmy mice) and Scotinomys (singing mice or brown mice), both comprised of 2 species (Musser and Carelton 2005). Scotin- omys is confined to premontane and montane moist forest in Central America, from Chiapas, Mexico, to western Panama. S. teguina occupies the northern and central parts of this range, whereas S. xerampelinus is restricted to Costa Rica and western Panama (Hooper 1972; Musser and Carleton 2005; Reid 1997). Areas of sympatry occur in Costa Rica, particularly the south- ern extent of the Central Cordillera such as Volca´n Irazu´, Volca´n Turrialba, and Volca´n Chiriqui, where the 2 species are segregated by altitude, ecology, and differences in vocal behavior (Hooper 1972; Hooper and Carleton 1976). The long calls of Scotinomys were described by Hooper and FIG.1.—Typical posture of male Scotinomys teguina associated Carleton (1976), including information for both S. teguina with stereotypic singing behavior. Both sexes of S. teguina and S. and S. xerampelinus, although a description of the vocaliza- xerampalinus exhibit similar posture during vocal displays. tions of females was presented for only S. teguina. The long call or ‘‘song’’ of Scotinomys is modulated temporally as well 1996; Zahavi 1980; see also Bradbury and Vehrencamp [1998] as in frequency and amplitude, and a sizeable fraction of the for a review). Thus, there is a trade-off among the social and songs’ energy is audible to the human ear. Individuals of both ecological benefits of producing localizable vocal signals, the species assume a characteristic posture while calling (Fig. 1): energetic costs associated with maintaining spectral character- reared up with neck extended and mouth agape (Hooper and istics that enhance propagation over distance, and the increased Carleton 1976; Reid 1997). The calls themselves are relatively risk of predation. This risk can be minimized when the fre- loud, and posturing contributes to acoustic resonant space quencies employed are above the hearing range of potential (Negus 1949). predators, typically meaning ultrasound. The 2 species of Baiomys occur at lower altitudes in drier, Ultrasound refers to frequencies above 15 kHz (Pye and more open habitats, including coastal prairie mixed scrub, post Langbauer 1998), although in the vernacular ultrasound tends to oak savanna, and mesquite–cactus from Texas to Mexico (B. refer to those frequencies above the upper threshold of human taylori—Eshelman and Cameron 1987), as well as arid weedy hearing (approximately 18–20 kHz; see for instance Hill and fields and dry brush throughout western and central Mexico Wyse 1989; see also Sales and Pye 1974:4). Vocal communi- (B. musculus—Packard and Montgomery 1978). There is only cation using ultrasonic frequencies has been routinely observed a small region of sympatry between the species of pygmy mice in a variety of muroid rodents (e.g., Galef and Jeimy 2003; Holy in west-central Mexico. In areas of overlap, the northern pygmy and Guo 2005; Lui et al. 2003; Moles and D’Amato 2000; Nyby mouse (B. taylori) occupies more grassy and xerophytic habi- and Whitney 1978; Okon, 1972; Sales and Pye 1974; tats than B. musculus, which ranges into zones with relatively Warburton et al. 1989). However, vocal signals within the higher humidity (Packard 1960). audible spectrum and with significant amplitude are rare in these Little is known about the vocal behavior of Baiomys. Blair taxa, possibly emphasizing their potential risk. Likewise, (1941:381) described the call of B. t. subater as a ‘‘high- although stereotypic vocalization, the use of ultrasound, and pitched, barely-audible squeal.’’ The call and posture assumed singing occur in a number of mammals, we know little about resembled the ‘‘singing’’ posture of Canis latrans, in that the these behaviors, their character, or function in mice. head appears ‘‘thrust forward and upward, stretching the The neotomine mice constitute a diverse assemblage of New throat’’ (Blair 1941:381), observations which were reiterated World rodents, within which several lineages are known for by Packard (1960). However Carleton (1980) noted that the vocalizations of varying complexity (Blair 1941; Hafner and call of Baiomys was ‘‘staccato-like,’’ similar to the song of December 2007 MILLER AND ENGSTROM—SINGING BAIOMYINE MICE 1449
Scotinomys. All descriptions of Baiomys vocalizations suggest signal/Mb. Although the input ratio reduces sampling audible frequencies. frequency by half, this recovers the frequency range of our Herein, we present the 1st comprehensive analysis of the microphone (to approximately 100 kHz). This ratio allows calls of B. musculus and B. taylori, as well as providing addi- capturing the duration of Scotinomys calls and recovers the tional data on the calls of S. teguina and S. xerampelinus. These complete range of the carrier frequency and a significant data contribute to an expanding taxonomic inventory of acous- proportion of the first 2 consecutive harmonic ranges. Samples tic behavior by the Neotominae. were subsequently converted to real time. Combining data on different, albeit equivalently calibrated, instruments can contribute nominally to variance around mea- MATERIALS AND METHODS surement mean values. However, the value ranges of data using A sample of 4–10 wild-caught males and females were either sampling strategy overlap significantly when interquar- examined for each species (Appendix I): B. musculus,5 tile data are plotted. We also assessed sampling equivalency by females, 4 males; B. taylori, 7 females, 6 males; S. teguina,8 means of pairwise t-tests, Wilcoxon signed-rank tests, or both females plus 2 additional F2 females, 8 males plus 4 additional for individuals that were sampled by either instrumentation F2 males; and S. xerampelinus, 4 females, 4 males plus 1 method (n ¼ 15). These tests indicate statistically insignificant additional F2 male. Individuals were observed and recorded in differences between alternative samples with regard to spectral the laboratories at the University of Toronto, Ontario, Canada; and temporal characteristics (Appendix II). The determination Angelo State University, San Angelo, Texas; and Centro de of between-species or within-species differences is therefore Educacio´n Ambiental e Investigacio´n Sierra De Hualtla, unaffected. Cuernavaca, Mexico. Periods of maximal acoustic activity Description of calls.—There are a variety of descriptive were identified by sampling acoustic behavior initially over the frameworks for categorizing vocal signals, each meant to facil- 24-h clock. Recordings were obtained from single individuals itate homologous comparison. However, Martin and Bateson housed separately. During experimental sessions focal animals (1993) recommend the use of neutral terms for describing were isolated from, but within hearing range of conspecifics, to behavior, so that function is not presumed. Because we know gather contextual data such as patterns of vocal reciprocity. nothing about the function of the stereotypic vocalizations of Samples ranged from 3 calls to as many as 50 calls per indi- the baiomyine mice a priori, we follow this example, and de- vidual, reflecting the variance in vocalizations produced by scribe the vocalizations in terms of their acoustic character (for individuals. One litter of B. musculus and several litters of instance a ‘‘chirp’’ as a single vocal element, versus a ‘‘strophe’’ Scotinomys were recorded during the course of our data collec- as a short collection of vocal elements of similar type), rather tion. We also recorded neonates and adult CD1 Mus musculus than by putative motivational identifiers (such as ‘‘alarm’’ or post hoc for comparative purposes (work in progress). ‘‘distress’’ calls). Recording was principally in real-time, using a model 4939 All recordings were digitized for analysis using 16-bit res- Bruel and Kjaer 0.25-inch dielectric free-field capacitance olution at a sampling rate of 192 kHz. High-pass band filters of microphone (Bruel and Kjaer, Nærum, Denmark), with a flat 500, 750, or 1,000 Hz were employed, depending on noise frequency response to 100 kHz, a sensitivity to 120 kHz, and sources in the recording environment, improving signal-noise with diminished sensitivity and mild attenuation of the higher resolution. We computed spectrograms using both Hamming frequencies. The microphone was suspended above the subject and Blackmann windows, initially at 512 then at 1,024 cage and positioned 30 cm from the cage floor. Microphone samples/block, with a window width of 70%. Frequency output was connected to either a Bruel and Kjaer model 2610 decomposition by fast Fourier transform using a Blackmann measuring preamplifier or a model ZE 0592 dual amplifier, window of 2048 band resolution generated power spectra for connected to a model 2807 power supply (Bruel and Kjaer). entire calls. Larger fast Fourier transform size was employed to Analog signal was converted to digital using a high-speed L-22 maximize fidelity in the spectral domain for frequency mea- sound card (Lynx Studio Technology Inc., Costa Mesa, Cali- surements. Calls were quantified for duration, complexity, and fornia), and CE Pro acoustic software (Syntrillium Software spectral dimensions, recording the following variables: call Corporation, Phoenix, Arizona), with sound output routed length and call complexity (number of notes or syllables), through a Eurorack MX 602A mixing board (Behringer Interna- minimum overall frequency (in kHz), maximum overall fre- tional, Willich, Germany). Analyses were conducted using the quency, peak frequency (frequency of maximum power over CE Pro analytical subroutines, as well as analytical subroutines the entire call), and overall bandwidth. These data allow for an of Raven (Cornell Lab of Ornithology, Cornell University, overview of both temporal and spectral domains and charac- Ithaca, New York) and SoundRuler (Center for Perceptual terization of each call in toto. Mean values per individual Systems, University of Texas, Austin, Texas) acoustic programs. sample for each parameter were calculated, such that statistical Data analysis reflects the efforts of 4 field seasons. Early analyses utilized only 1 value per individual animal to avoid samples of Scotinomys were recorded through time expansion pseudoreplication. using a Portable Ultrasound Processor (Ultra-Sound Advice, Distribution of univariate data was assessed using normal Wimbleton, London, United Kingdom), with a 3-Mb buffer probability plots and histograms, and Levene’s statistic was capacity. We sampled at a frequency of 448 ks/s, with a used to assess overall heteroscedasticity. However, many formal compression–expansion ratio of 2:10, yielding 4.46 s of tests for equality of standard deviation lack robustness against 1450 JOURNAL OF MAMMALOGY Vol. 88, No. 6 nonnormality. We therefore also assessed among-group vari- formant (harmonic) frequencies are clearly observed, with ability following Moore and McCabe (1993:723, 727; maxi- strong peaks that demonstrate a more-or-less linear decay in mum/minimum SD 2). Although a conservative estimator, the power from the carrier harmonic. In Baiomys, the moment parametric procedures to which this assumption applies are bandwidth (relative bandwidth at any moment, position, or generally robust to moderate variation in standard deviations. interval within a pulse) is significantly narrower than that for We visualized relative dimorphism within species by means either species of Scotinomys, which have a steeper slope of of a dimorphism index of male/female values. An index value frequency change and are thus relatively more broadband of 1.00 represents absolute monomorphism, whereas values (Tables 1 and 2). above 1 indicate larger measurements in males, and values less All 4 species produce calls consisting of complex series of than 1 indicate larger measurements in females. Statistical sig- frequency-modulated pulses (Figs. 2–4), each pulse beginning nificance was determined from raw individual values (i.e., in the 30- to 50-kHz bandwidth and falling to lower fre- nonratios) using independent samples t-tests, with assumptions quencies. However, the species differ in temporal and spectral of equal variance and normal distribution assessed as above. aspects of their calls (Figs. 5 and 6; Table 2). Characters that We recognize here the limitations of the Portable Ultrasound distinguish the 2 genera include frequency minimum, peak Processor system with regard to memory capacity and process- frequency, and calculated emission rate, the number of notes ing. For instance, calls of Scotinomys often are introduced by emitted over unit time (n/s), averaged over the total length a small number of quiet, low-amplitude notes that the Portable (duration) of the song (NN/TD). Differences in emission Ultrasound Processor system may not recover as consistently. rates characterize both species of Baiomys with less acoustic Likewise, although the occurrence of extremely long calls in packing per unit time than Scotinomys (B. taylori: 9.19 6 0.74; S. teguina males (.14 s) is infrequent and thus represents B. musculus: 8.27 6 1.05), and S. xerampelinus appears to extreme observations, such calls are not captured in our use have a slightly faster emission rate (14.24 6 1.22) than of the Portable Ultrasound Processor system. As such, our S. teguina (12.72 6 1.16). Characters that further differentiated estimation of dimorphism in S. teguina is conservative. the species include bandwidth, maximum frequency, note We then assessed among-species differences. When vari- number, and total duration. Three of these characters (song ables were sexually dimorphic, we assessed samples of males duration, pulse number, and bandwidth use) especially set apart and females separately. Where pooled samples of males and S. teguina (Tables 1 and 2), with S. xerampelinus being more females were normally distributed and variance was homoge- similar to either species of Baiomys than to S. teguina. neous, we performed parametric analysis of variance (ANOVA) Additionally, some baiomyines are dimorphic in their vocal- to assess univariate measurements, with post hoc pairwise izations, but the degree of dimorphism varies among species. control of error rate using Tukey’s honestly significant differ- This ranges from monomorphism in B. taylori to pronounced ence. When parametric assumptions were not met, we used dimorphism in S. teguina. a nonparametric Kruskal–Wallis test, with Bonferroni correc- Scotinomys.—Scotinomys is characterized by repetitive and tion adjusting for post hoc multiple contrasts (a , 0.005, for 9 complex vocal signals that are modulated in frequency, independent contrasts). All statistical analyses were performed amplitude, and time (Figs. 5 and 6), herein termed ‘‘songs’’ using SPSS version 14.0 (SPSS Inc., Chicago, Illinois). Results (after Hooper and Carleton 1976:17; see also Figs. 3, 7, and 8). are reported as mean 6 SD. Although both baiomyine genera begin song pulses in the We used principal component analysis to assess the overall ultrasonic frequencies, Scotinomys invests a significant amount pattern of dispersion of entire vocalizations in multivariate space of song energy in the audible spectrum (Figs. 2, 3, and 6). (NTSys version 2.1, Applied Biostatistics, New York, New Overall, frequency sweeps range from approximately 8 to 50 York), using the covariance matrix based on standardized data. kHz, and songs range from approximately 1 to 16 s in duration, Scree plots were examined and a broken-stick model was consisting of roughly 10–170 notes. Each song represents employed, resulting in the reduction of dimensionality of the data a pulse train where modulation over its course, in terms of set to 2 principal components, represented by bivariate plots. This frequency maxima and minima, varies individually from being analysis contributes a holistic perspective of calls with which to nonconstant to highly stereotyped (Fig. 6). In S. teguina, examine aspects important to species and sexual identity. frequency bandwidth is more or less internally constant in the All research on live animals conformed to guidelines pulse train, but with variation at either the introduction or approved by the American Society of Mammalogists (Gannon terminal ends. Bandwidth tends to widen toward signal et al. 2007), and was approved by 2 independent institutional terminus in S. xerampelinus (Figs. 6–8). Overall, the song animal care and use committees (protocols 20004234 and patterns vary between individuals, with some members of both 20005977, Department of Ecology and Evolutionary Biology, species being more stereotyped in their use of frequency. University of Toronto; and protocol 2004-021, Royal Ontario There is evidence of sexual dimorphism in both spectral and Museum [ROM] Animal Care Committee). temporal features. However, spectral differences between sexes, illustrated by the dimorphism index, are subtle, and generally not statistically significant. There is pronounced RESULTS sexual dimorphism in the vocalizations of Scotinomys in tem- Spectral and temporal features of the long calls of Baiomys poral characters, especially S. teguina (Tables 1 and 3). and Scotinomys are characterized in Table 1. In all species, Although S. teguina demonstrates the largest degree of December 2007 MILLER AND ENGSTROM—SINGING BAIOMYINE MICE 1451
TABLE 1.—Descriptive statistics for acoustic parameters measured over entire calls of Baiomys and Scotinomys. Overall means are based on individual sample means for either sex, with the number of individuals in parentheses. The total number of calls analyzed appears after sex, in parentheses. Frequency in kilohertz (kHz). Bandwidth modulation represents bandwidth of the frequency sweep across calls. Range reports minimum and maximum values over total call samples. Individual data are available upon request.
Variable Species Sex (n calls) X 6 SD (sample n means) Range Total duration (s) B. musculus Male (140) 2.535 6 0.220 (4) 1.157 3.436 Female (130) 2.396 6 0.441 (5) 2.422 2.590 B. taylori Male (144) 1.886 6 0.657 (6) 0.422 7.580 Female (169) 1.995 6 0.399 (7) 0.804 4.948 S. teguina Male (346) 9.220 6 0.869 (12) 3.753 18.073 Female (247) 6.428 6 0.970 (10) 1.063 9.774 S. xerampelinus Male (152) 2.578 6 0.267 (5) 1.393 3.844 Female (120) 1.832 6 0.104 (4) 0.890 2.696 Pulse number B. musculus Male (140) 20.903 6 2.561 (4) 5 29 Female (130) 20.118 6 6.201 (5) 9 31 B. taylori Male (144) 17.110 6 6.440 (6) 3 47 Female (169) 18.757 6 3.245 (7) 7 44 S. teguina Male (346) 113.384 6 8.296 (12) 60 174 Female (247) 84.375 6 13.465 (10) 20 118 S. xerampelinus Male (152) 35.574 6 4.497 (5) 9 53 Female (120) 27.053 6 2.088 (4) 18 43 Minimum frequency (kHz) B. musculus Male (140) 27.464 6 1.053 (4) 17.910 30.460 Female (130) 25.831 6 1.508 (5) 21.870 35.970 B. taylori Male (144) 21.266 6 0.975 (6) 16.600 24.510 Female (169) 21.261 6 1.815 (7) 17.960 26.170 S. teguina Male (346) 10.451 6 1.450 (12) 7.125 14.760 Female (247) 11.010 6 1.481 (10) 7.697 14.060 S. xerampelinus Male (152) 10.434 6 1.260 (5) 7.968 13.120 Female (120) 11.677 6 1.704 (4) 8.671 15.000 Maximum frequency (kHz) B. musculus Male (140) 47.818 6 2.243 (4) 36.090 57.610 Female (130) 49.463 6 2.823 (5) 44.140 58.980 B. taylori Male (144) 39.592 6 2.899 (6) 29.490 47.070 Female (169) 39.869 6 2.235 (7) 32.610 48.630 S. teguina Male (346) 42.063 6 2.384 (12) 32.060 51.358 Female (247) 40.090 6 3.359 (10) 31.300 48.510 S. xerampelinus Male (152) 34.252 6 1.780 (5) 26.900 41.440 Female (120) 34.374 6 3.039 (4) 24.060 43.120 Peak frequency (kHz) B. musculus Male (140) 36.453 6 1.194 (4) 22.850 34.370 Female (130) 37.133 6 1.406 (5) 33.000 41.790 B. taylori Male (144) 30.027 6 1.731 (6) 26.130 47.460 Female (169) 30.079 6 1.345 (7) 24.600 34.470 S. teguina Male (346) 23.875 6 2.831 (12) 14.250 41.430 Female (247) 23.205 6 2.331 (10) 14.430 35.780 S. xerampelinus Male (152) 16.598 6 1.005 (5) 12.180 21.280 Female (120) 18.021 6 2.634(4) 13.350 28.280 Bandwidth modulation B. musculus Male (140) 20.354 6 3.196 (4) 7.770 31.930 Female (130) 23.632 6 2.780 (5) 15.200 32.790 B. taylori Male (144) 18.325 6 2.697 (6) 8.400 27.150 Female (169) 18.687 6 2.157 (7) 12.110 25.390 S. teguina Male (346) 31.613 6 2.475 (12) 22.123 43.858 Female (247) 29.097 6 3.793 (10) 22.863 39.185 S. xerampelinus Male (152) 23.818 6 1.508 (5) 15.650 32.847 Female (120) 22.697 6 1.362 (4) 13.750 29.300 dimorphism in absolute terms for these measurements, it is in the number of notes emitted per unit time, averaged over the equivalent to S. xerampelinus in relative terms, with long-call total length of the song (NN/TD). vocalizations of males of both species approximately 40% There are significant differences between S. teguina and S. longer in duration, on average, than those of females (S. xerampelinus in all univariate parameters, with the exception of teguina: t ¼ 7.20, d.f. ¼ 20, P , 0.0001; S. xerampelinus: t ¼ minimum frequency (Tables 1 and 2). However, each pulse of 5.22, d.f. ¼ 7, P ¼ 0.001) and with 34% more notes or pulses the complex pulse train of these mice modulates rapidly to its per call in males than in females (S. teguina: t ¼ 6.20, d.f. ¼ frequency minimum, which is significantly less than the pulse 20, P , 0.0001; S. xerampelinus: t ¼ 3.47, d.f. ¼ 7, P ¼ maximum frequency. Minimum frequencies in both species of 0.009). No significant dimorphism was evident in either species Scotinomys average 10–12 kHz, but maximum frequencies 1452 JOURNAL OF MAMMALOGY Vol. 88, No. 6
FIG.2.—Spectrogram and power spectra for Baiomys musculus and B. taylori. Frequency is given in kHz, with 18–20 kHz representing the approximate boundary between audible and ultrasonic acoustic spectra. A) Baiomys musculus ROM 117128 (female); B) B. musculus BmX (male); C) B. taylori ROM 117148 (female); D) B. taylori ROM FIG.3.—Spectrogram and power spectra for Scotinomys xerampe- 117145 (male). Power spectra are denoted in relative amplitude, with linus and S. teguina.A)Scotinomys xerampelinus ROM 117709 increasing negative values representing logarithmic decay from (female); B) S. xerampelinus ROM 117708 (male); C) S. teguina maximum power. The spectral peak represents frequency range of ROM 116832 (female); D) an equivalent 4-s segment of S. teguina maximum power, paired to the frequency scale on the y-axis of the ROM 117155 (male). Power spectra are denoted in relative amplitude, corresponding spectrograms. The carrier harmonic is represented in with increasing negative values representing logarithmic decay from the tallest peak, wherein the carrier bandwidth for Baiomys is maximum power. The spectral peak represents frequency range of significantly narrower than for either species of Scotinomys. maximum power, paired to the frequency scale on the y-axis of the corresponding spectrograms. The carrier harmonic is represented differ between species (Tables 1 and 2), ranging from a mean in the tallest peak, and the carrier bandwidth for Scotinomys is of 34.31 6 2.25 kHz in S. xerampelinus to 41.17 6 2.97 kHz significantly broader than for either species of Baiomys, with minima in S. teguina. Overall bandwidth is therefore broad across calls, clearly below 20 kHz. and is broadest in S. teguina (S. teguina versus S. xerampe- linus: t ¼ 8.29, d.f. ¼ 29, P , 0.0001, equal variance not assumed). Overall differences in frequency and bandwidth above the audible spectrum. Both species of Baiomys employ (Tables 1 and 2) also indicate that species use different spec- a relatively narrow overall bandwidth during the course of their tral ranges. calls as compared to either species of Scotinomys, and are In both sexes, S. teguina exceeds the values of S. characterized by higher minimum frequencies (range 22–30 xerampelinus for both the temporal measurements of total kHz). Of the 2 species, the songs of B. musculus occupy the duration and note number. S. teguina has a longer call, the higher end of this range (Table 2). The upper end of the duration of which significantly exceeds that of S. xerampelinus bandwidth (in kHz) used by Baiomys is lower in B. taylori (39.59 and Baiomys by 2–3 times in females (Figs. 5, 8, and 9A) and 6 2.88 for males, 39.87 6 2.24 for females) than in B. musculus 3–4 times in males (Table 2; Figs. 4, 5, and 9B). The call is (47.82 6 2.24 for males, 49.46 6 2.83 for females). The highest complex in S. teguina, in terms of note number, particularly in frequencies are attained by B. musculus, and there is significant males (Fig. 4). The increased number of notes results, in part, overlap between B. taylori and S. teguina (Tables 1 and 2). from the overall increase in call duration, where there is a Songs in Baiomys also are shorter in duration than in strong correlation (Scotinomys: Spearman’s rho ¼ 0.964, P , Scotinomys, with fewer syllables (compare Figs. 7 and 8 to 9A 0.0001, n ¼ 859). Variance in pulse number is greatest in and 9B). However, there is more variation between syllables S. teguina, suggesting that the temporal complexity of calls is in Baiomys than appears in the calls of Scotinomys. Thus, in more variable in this species. Although S. teguina represents Baiomys the call is more complex in form albeit less complex a larger sample, increased variability also was evident when in terms of overall repetition rate. The pattern of frequency reduced subsamples, randomly selected, were contrasted. modulation over the course of the pulse train is not constant but Baiomys.—The repetitive and complex vocal signals of curvilinear in progression in either species (Fig. 6). Graded Baiomys are modulated in frequency, amplitude, and time (Figs. temporal change is evident within songs, in terms of both the 2, 5, and 9). In these characteristics, their long calls resemble interval between syllables and syllable duration. those of Scotinomys. However, the spectral range used by There are no significant differences in temporal character- Baiomys, both in frequency maximum and minimum, is entirely istics of song in either species, and both species are generally December 2007 MILLER AND ENGSTROM—SINGING BAIOMYINE MICE 1453
TABLE 2.—Tests of significance for univariate acoustic measure- ments reporting either ANOVA F-statistic or Kruskal-Wallis chi- square statistic. Where measurements are sexually dimorphic among taxa, tests of male and female means are reported independently. Subsets are grouped according to significant differences. Patterns of taxonomic subsets reflect comparisons of nonoverlapping ranges of standard error about the mean, alpha ¼ 0.05. TD ¼ total duration; NN ¼ pulse number; FMIN ¼ overall frequency minimum; FMAX ¼ overall frequency maximum; TPEAK ¼ overall peak, or maximum amplitude frequency; and BW ¼ modulation bandwidth. St ¼ Scotinomys teguina,Sx¼ S. xeramelinus,Bm¼ Baiomys musculus, Bt ¼ B. taylori.
Variable Sex F (df) v2,(d.f.) P Subsets TD Male 226.262 (3, 23) , 0.0001 (Bm, Bt, Sx) (St) Female 84.045 (3, 22) , 0.0001 (Bm, Bt, Sx) (St) FIG.4.—Entire spectrogram of the song of Scotinomys teguina NN Male 388.231 (3, 23) , 0.0001 (Bm, Bt) (Sx) (St) ROM 117155 (male). The 4-s segment appearing in Fig. 3 represents Female 97.248 (2, 22) , 0.0001 (Bm, Bt, Sx) (St) the middle one-third of this song, from the 6- to the 10-s marks. Total FMIN Pooled 40.666 (3) , 0.0001 (Bm) (Bt) (St, Sx) duration ¼ 11.115 s, total number of notes ¼ 130, carrier bandwidth FMAX Pooled 44.816 (3, 49) , 0.0001 (Bm) (Bt, St) (Sx) from 6.937 kHz to 42.930 kHz. PEAK Pooled 168.772 (3, 49) , 0.0001 (Bm) (Bt) (St) (Sx) BW Pooled 42.078 (3) , 0.0001 (Bt) (Bm, Sx) (St) bution of females, which in the pooled multivariate data most closely approximate the distribution of male S. teguina. sexually monomorphic in call parameters. However, B. Clusters (analyses of males and females) corresponding to S. musculus is weakly dimorphic in minimum frequency (t ¼ xerampelinus are equidistant from both S. teguina and Baiomys 3.09, d.f. ¼ 7, P ¼ 0.018), with a dimorphism index value of in both PCA1 and PCA2, reflecting the intermediate status 1.063. The dimorphism index for bandwidth is relatively large of this species in temporal character, as well as its lower in B. musculus (0.861), but also not statistically significant. maximum and peak frequencies. Minimum, maximum, and peak frequencies can be used to Strong positive loadings on the 1st principal component distinguish between species of Baiomys; however, temporal indicate songs of increasing length and complexity, distin- characters and overall emission rate cannot (Tables 1 and 2). guishing the 2 genera, but likewise distinguishing species The expected positive relationship between call length and within genera. In contrast, strong positive loadings on the 2nd pulse number, although evident across all baiomyine species component for minimum and peak frequency reflect greater (Spearman’s rho ¼ 0.911, P , 0.0001, n ¼ 1416) is, however, investment in the ultrasonic acoustic spectrum, either by means weakest in the pygmy mice (Baiomys: Spearman’s rho ¼ of increasing bandwidth to include higher frequencies (S. 0.832, P , 0.0001, n ¼ 557). Overall emission rates for neither species are sexually dimorphic. teguina) or by increasing the frequency minimum that, in part, Principal component analysis.—In multivariate space, indi- defines the bandwidth used (Baiomys). viduals clustered into 4 groups corresponding to species Additional vocalizations.—During male–female contact (Fig. 10). Data dispersal in both sexes is similar in multivariate encounters, we recorded low-amplitude, individually piped space. The first 2 principal component axes (PCA1 and PCA2) notes as well as short pulse trains of similarly muted frequency- account for the majority of variation (Table 4). Total duration, modulated sequences, or ‘‘strophes.’’ These were weaker, but number of notes, and minimum frequency have the largest load- more tonal than notes comprising the typical song. Strophes ing values on PCA1, whereas maximum and peak emphasized made under these circumstances bear some superficial simi- frequency have the largest loading values on PCA2. This is larity to the song, but there are differences that distinguish the to be expected because the calls of both species of Scotinomys 2. Strophes are characterized by more irregular modulation, and appear more densely packed with regard to number of notes are most often restricted to higher frequencies. We also per unit time than are the songs of either species of Baiomys. identified variation in emission rates within strophes, as well as The distinct nature of the call of S. teguina is evident by its distinct modulation forms (Fig. 11). separation from S. xerampelinus and Baiomys, on both PCA1 Neonates of the baiomyines recorded (B. musculus, S. and PCA2 (Fig. 10). Also, clusters representing the 2 species teguina, and S. xerampelinus) produce a restricted number of of Baiomys are more homogeneous by sex with less apparent vocalizations, the most common of which is the audible chirp. dimorphism than the 2 species clusters of Scotinomys. Occurring frequently in long trains while in the nest, they carry Dispersal patterns within S. teguina are affected in part by roughly between 4.5 and 7.5 kHz and are of a lower frequency the presence of an outlying sample (female, ROM 116808), than the long vocalizations of adults. These stronger vocal corresponding to an F2 generation individual. Likewise, the 2 signals range from being relatively tonal, to more coarsely females from the locality of Escazu, near Pico Blanco (ROM broadband and noisy. Aroused states result in long series of 117157 and 116832), occupy the upper limits of the distri- chirps in which higher harmonic structure is more distinct. The 1454 JOURNAL OF MAMMALOGY Vol. 88, No. 6
FIG.5.—Oscillograms for A–D) Baiomys, and E–H) Scotinomys, with time represented on the x-axis and power on the y-axis. Note the difference in time scales on the x-axis, which were selected to be able to display the shorter songs of Baiomys with the longer songs of Scotinomys. Amplitudes represent relative rather than absolute power, because of variation in instrumentation, and difficulties in calculating the exact distances to a subject. Baiomys taylori: A) female, B) male; B. musculus: C) female, D) male; Scotinomys xerampelinus: E) female, F) male; S. teguina:G) female, H) male. All oscillograms are of the same individuals presented in Figs. 3 and 4, and correspond to those spectrograms. Oscillograms for S. teguina demonstrate the increasing power envelope from beginning to terminus, a pattern generally characteristic for both species and sexes of Scotinomys, but that is less pronounced in S. xerampelinus. chirp is similar to that observed in adult mice during contact piping notes bear a striking resemblance to the calls of sep- interactions, in particular same-sex interactions. arated neonatal M. musculus, which we have recorded from the In addition to the audible chirps (Fig. 12A), there are pulses CD1 laboratory strain of M. musculus (Fig. 12D). of frequency-modulated notes emitted by both B. musculus and S. teguina (Figs. 12B and 12C). These occur as single notes, in couplets, or in short strophes with a frequency range of DISCUSSION approximately 40–30 kHz. Although less complex, infant calls Song.—We provide the 1st quantified analysis of acoustic share similarities to the songs of adult Baiomys, and bear the communication by baiomyine mice. The principal vocaliza- rudiments of the elongated song of adult Scotinomys. These tions of both Baiomys and Scotinomys are pulse trains of December 2007 MILLER AND ENGSTROM—SINGING BAIOMYINE MICE 1455
FIG.6.—Frequency modulation over interval time for A and B) maximum and C and D) minimum frequency in A and C) Baiomys and B and D) Scotinomys. Note the difference in y-axis scale between genera, in accordance to respective frequency spread. Intervals represent sequentially, the 1st, 3rd, 5th, 10th, 15th, 20th, 25th, 30th, 35th, and 40th notes, then every 10th note thereafter until the termination of the song. The last interval on respective x-axes represents the last note. The number of intervals present in each species reflects the relative song length. Bars represent total species’ means 6 SD of a randomly selected call for each individual in the species sample. Species are monomorphic in either variable depicted and sample means are pooled for sexes. similar notes that resemble a simple polysyllabic, 1st-order and continuous, as opposed to disjunct or patterned. As such sequence (after Broughton 1963). However, careful examina- these calls retain syllabic identity, but as a single phrase. They tion reveals progressive modulation in power, frequency, and are therefore best described as continuous, multisyllabic songs. time over the duration of the signal. Because syllables vary, Songs can be distinguished from calls by being longer in albeit in either a graded or progressive manner, these vocal- duration and more complex. Hauser (1997) also posits that izations can be defined as ‘‘song’’ (Broughton 1963:882; song is most commonly used in competitive situations, notably Hooper and Carleton 1976:17; see also Holy and Guo 2005). in the competition for resources and mates. There are numer- As such, they conform to the classic concept of song as ous studies of avian vocal behavior that support the idea that a ‘‘recognizable sequence or pattern of notes of more than one song complexity and production is influenced by female kind’’ (Thorpe 1961:38). In Scotinomys, syllabic distinction choice, thus generating sexual selection (Andersson 1994; is predominantly temporal, when considering total syllable Eriksson and Wallin 1986; Johnson and Searcy 1996; Nowicki number. However, the lower frequency limit of each modulated and Searcy 2004). Mating signals should be more expensive, note generally reduces as songs progress. Modification of in terms of fitness, if they are reliable targets of selection syllable maximum frequency also occurs, with a single direc- (Andersson 1994). tion of change in S. xerampelinus, and a tendency for bidi- Singing behavior has only been described and documented rectional change in S. teguina at either end of the song (Fig. 6). in a few mammals. Principal examples include the hump- In Baiomys, syllables are more distinctively graded in the back whale, Megaptera novaeangliae (Payne and McVay spectral domain. Although baiomyine signals do not share the 1971; Thompson et al. 1979), sac-winged bats (Saccopteryx phrases or motifs notable in recently described songs of males bilineata—Behr and von Helversen 2004; Davidson and of the BALB/c strain of M. musculus (Holy and Guo 2005), Wilkinson 2004), false vampire bats (Cardioderma cor— the complex nature of note modulation complies both with McWilliam 1987), and some primates, most notably the Broughton’s definition of ‘‘song,’’ as a ‘‘sound of animal origin duetting of gibbons such as Hylobates klossii, H. lar, and which is not both accidental and meaningless,’’ as well as Symphalangus syndactylus (e.g., Chivers and Gittins 1978; Thorpe’s definition of ‘‘a series of notes [or syllables], Cowlishaw 1992; Raemaekers et al. 1984). Singing behavior in generally of more than one type, uttered in succession and so mice has attracted significant attention, particularly regarding related as to form a recognizable sequence or pattern in time’’ its putative function in reproductive behavior (Holy and Guo (Broughton 1963:882; Thorpe 1961:15). Modulation is gradual 2005; Nyby and Whitney 1978; Nyby et al. 1979, 1981; White 1456 JOURNAL OF MAMMALOGY Vol. 88, No. 6
FIG.7.—Complete, expanded spectrogram of female Scotinomys teguina ROM 117151 in real time. The spectrogram demonstrates varying frequency and temporal modulation through the course of the song, as well as harmonic structure. Total duration ¼ 6.119 s, number of notes ¼ 82, bandwidth ranges from 8.531 kHz to 33.750 kHz. et al. 1998). However, complex vocal signals have been known Cartago), and include a sample of S. teguina from the foothills to occur in a variety of distantly related rodent species as well of Escazu. These latter mice are somewhat smaller in size as in some insectivores (Sales and Pye 1974). The phenomenon than other populations and exhibit more aggressive tendencies of stereotypic ‘‘song,’’ or signaling, is likely more widespread in captivity. Call duration of mice originating from this region than currently appreciated. is more variable, a distinction not unlike the Nicaraguan sam- Our data reaffirm those of Hooper and Carleton (1976) ple described by Hooper and Carleton (1976). Variability in regarding the general features, similarities, and dissimilarities S. teguina may therefore reflect random geographical variation between the 2 species of Scotinomys. In general features, S. or contextual adaptation. This variation and a greater repre- teguina calls are longer, more complex, and modulated over sentation of vocalizations by females in our study likely a broader bandwidth than songs of S. xerampelinus (Table 1). contribute to differences in the 2 data sets. Here we provide the Our study sample included mice from localities also sampled 1st complete exemplar spectrograms for females of either by Hooper and Carleton (Volca´n Irazu´, various localities in species (Figs. 7 and 8). Hooper and Carleton (1976) also
FIG.8.—Complete, expanded spectrogram of female Scotinomys xerampelinus ROM 117709 in real time. The spectrogram demonstrates varying frequency and temporal modulation through the course of the song, however, with less overall complexity than is demonstrated by S. teguina. Total duration ¼ 2.291 s, number of notes ¼ 29, bandwidth ranges from 13.680 kHz to 38.060 kHz. December 2007 MILLER AND ENGSTROM—SINGING BAIOMYINE MICE 1457
TABLE 3.—Relative dimorphism (male/female) based on overall TABLE 4.—Eigenvalues of normalized data, percentage of total means of individual mean values for call variables per species of variation, and vector loading values of the parameters total duration, Baiomys and Scotinomys (total duration [TD]; pulse number [NN]; note number, frequency minimum, frequency maximum, peak minimum frequency [FMIN]; maximum frequency [FMAX]; peak frequency, and bandwidth for the first 2 principal components in the overall frequency [TPEAK] or maximum amplitude frequency; and principal component analysis for the pooled data set. Cumulative bandwidth modulation [BW]), where monomorphism equals 1.000. percent of total variation is given in parentheses after principal Values greater than 1 indicate males . females, and values less than 1 component 2 values. indicate females . males. Greater deviations from 1.00 indicate larger magnitudes of sexual difference. Values in bold denote significant Parameter Principal component 1 Principal component 2 differences in means between males and females, as determined by Eigenvalue 0.344 0.132 independent sample t-test, with a Bonferroni correction for multiple % of total variance 68.35 26.56 (94.56) comparisons (P 0.002). Total duration 0.4520 0.3614 Number of notes 0.5308 0.3078 Variable B. musculus B. taylori S. teguina S. xerampelinus Frequency minimum 0.5327 0.3320 Frequency maximum 0.1077 0.5860 TD 1.058 0.945 1.434 1.406 Peak frequency 0.3293 0.5108 NN 1.039 0.912 1.344 1.315* Bandwidth 0.3319 0.2452 FMIN 1.063 0.999 0.941 0.894 FMAX 0.967 0.993 1.042 0.996 TPEAK 0.982 0.998 1.029 0.921 BW 0.861 0.981 1.086 1.078 that represents acoustic ‘‘dead space.’’ Thus, there is greater RATE (NN/TD) 0.991 0.938 0.937 0.931 acoustic ‘‘packing’’ in Scotinomys than in Baiomys, with an * P ¼ 0.009. average rate of pulse emission in Scotinomys more than 50% greater than within the song in Baiomys. Variation in complexity, as measured by emission rate, recognized that, despite their characteristic high frequencies, clearly distinguishes the 2 genera and also species within the songs of Scotinomys propagate well in the field. This sug- Scotinomys. Emission rate is slightly slower in S. teguina than gests an investment of significant energy. We concur, because in S. xerampelinus. Because the songs of both species are we have been able to detect signals at .5 m in the laboratory temporally modulated, this lower rate of emission may in part and up to 5 m for songs broadcast in various habitats with our be a product of temporal scaling, reflecting the effect of instrumentation. significant call elongation in S. teguina. This phenomenon may Scotinomys versus Baiomys.—Although there are notewor- also, in part, explain sexually dimorphic features in the songs thy similarities between vocalizations of Baiomys and Sco- of Scotinomys. Although S. teguina demonstrates the largest tinomys, there are also important differences. Vocalizations of absolute degree of dimorphism in temporal features, it is both genera are characterized by pulse trains of individual equivalent to S. xerampelinus in terms of relative call length. notes, or syllables, that are individually modulated in pitch. Thus, the appearance of increased dimorphism in S. teguina These high-to-low frequency sweeps constitute principal relative to S. xerampelinus is likely attributable to allometry. frequency modulation, and characterize all species. Overall, The most significant difference between the 2 genera is in however, syllables vary in both duration and pitch from the the bandwidth extremes of the acoustic spectrum habitually onset of the call to its termination (Fig. 6). This variation in used. Crudely differentiated, these represent the ultrasonic and pitch across successive notes in a pulse train compounds audible (sonic) spectrum (Pye and Langbauer 1998; see also principal frequency modulation, and is herein termed 2nd-order Hill and Wyse 1989; Sales and Pye 1974:4). Although frequency modulation (frequency modulation over time). In anthropocentric in definition, ‘‘ultrasound’’ maintains biolog- part it reflects a changing functional bandwidth over the ical significance in that frequencies of these magnitudes are duration of the song experienced by all species (Fig. 6). also above the peak hearing sensitivities of many potential Temporal modulation of the pulse train appears most pro- predators of mice, such as raptorial birds. nounced in S. teguina, and may represent a scaling phenom- Most birds, in particular birds of prey, are insensitive to enon reflecting the large magnitude of call elongation that ultrasound, and have variably reduced sensitivities to frequen- discriminates S. teguina among the Baiomyini: in essence, the cies above 2–6 kHz (Dooling 1991; Edwards 1943; Klump longer the call, the more exaggerated the modulated change by et al. 1986; Sales and Pye 1974; Schwartzkopff 1955). Higher the termination of the song. frequencies also are less likely to be seismically propagated, We also interpret song complexity in terms of duty cycle: the important when predators (e.g., snakes) can potentially detect average rate of notes over the course of the song (Bee and vibrations in the substrate. In Baiomys, the entire call is Gerhardt 2001; Crocroft and Ryan 1995; Morris 1980). Both generally produced at frequencies greater than 20 kHz. genera differ in this characteristic. Unlike Scotinomys, Baiomys Although a proportion of the S. teguina song, regardless of is generally monomorphic in its song and, despite durations of sex, is above the 20 kHz mark, minimum and peak frequencies similar length to S. xerampelinus, there are fewer syllables in can range substantially lower. In S. xerampelinus, the full range the pulse train. The relative lack of numeric complexity in of peak and minimum frequencies occupy the audible Baiomys suggests less energy investment in vocal activity, as spectrum. An increased risk of predation correlated with the opposed to the temporal fraction between notes and phrases production of song was noted by Hooper and Carleton (1976). 1458 JOURNAL OF MAMMALOGY Vol. 88, No. 6
FIG.9.—Complete, expanded spectrogram of female Baiomys taylori ROM 117148 and male B. musculus BmX in real time. Both calls demonstrate less densely packed signals compared to Scotinomys, per unit time. Both frequency and temporal modulation are evident through the course of the songs. A) female B. taylori; B) male B. musculus. A) Total duration ¼ 2.151 s, number of notes ¼ 19, bandwidth ranges from 19.820 kHz to 39.160 kHz. B) Total duration ¼ 3.003 s, number of notes ¼ 25, bandwidth ranges from 26.950 kHz to 48.430 kHz.
Loud, low-frequency calls travel farther and are more easily ecological profiles of each of the baiomyine species are detectable than ultrasound, and selective use of frequency has required to address questions about the costs and benefits of been speculated to serve a possible role in predation avoidance signaling strategies. (e.g., Wilson and Hare 2004). However, more detailed Other vocalizations.—In addition to the song and the chirp, we found previously unreported vocalizations in each genus. These sequences constitute unique vocalization categories in the Scotinomys repertoire, ranging from single modulations to more complex series (strophes). We therefore term the stereotypic song as type I and these strophes as type II frequency-modulated signals, the latter of which possess distinct variants. We also report the 1st observations of frequency-modulated ultrasound in baiomyine infants. Detailed analyses are limited by sample size, but we draw attention to similarities between these infant vocalizations and one variant of the 2nd type II adult vocalization, documented herein. For infant mice, separated from a parent, frequency- modulated pure tones would provide an ideal mechanism for localization. Playbacks of these vocalizations frequently elicit vigorous searching by parental mice (Allin and Banks 1971; Sales and Smith 1978; Sewell 1970; Smith 1976; see also Ehret FIG. 10.—Principal component analysis of call variables, with axes 1992). In Mus, these calls generally disappear in adult mice, scaled according to sample variance explained by each component. and are emitted mainly during copulation. There are a limited 0 ¼ males, 1 ¼ females. Genera are distinguished on principal component axis 1 and species separate on principal component axis 2. number of cases where vocalizations forming part of the Sexes segregate in multivariate space in Scotinomys, and to a lesser neonatal or juvenile vocal repertoire persist in adult mammals. degree in Baiomys musculus. However in B. taylori, sexes are nearly These include whining behavior in canids (Cohen and Fox homogeneous, consistent with lack of sexual dimorphism in the song 1976), the whistles of raccoon cubs (Sieber 1984), the pip call of that species. of the juvenile Egyptian mongoose (Ben-Yaacov and Yom-Tov December 2007 MILLER AND ENGSTROM—SINGING BAIOMYINE MICE 1459
FIG. 11.—Type II frequency-modulation variants recovered from adult male–female dyad experiments: variant 1, variant 2, variant 3. Both subjects here belong to Scotinomys teguina. Dyad experiments allowed for direct contact between subjects; however, some variants were recovered when subjects were physically separated, but within potential visual and olfactory contact.
1983; Du¨cker 1960; see also Estes 1991), and the nest-chirp of variants. Audible vocalizations additionally occur in all species the African civet (Ewer and Wemmer 1974). In baiomyines, the during paired encounters. In Baiomys, the frequency difference call structure and behavior of adults suggests the retention of between the minimum frequency of these short chirps and the an element of the neonatal repertoire, gaining energy and minimum frequency employed by the adult Baiomys call repetition in adulthood. The ultimate function is retained suggests that the 2nd harmonic may also be suppressed in this (localization tool), but the proximate motivation is novel. genus during song. Frequency dispersion.—The carrier frequency of baio- This marks a dichotomy in vocal behavior: all baiomyines, myines (being the frequency in which the most energy is and in particular Baiomys, are capable of using lower invested and thus also the frequency of greatest biological frequencies than those that characterize their stereotyped call. significance to the receiver) appears to represent the formant Selective use of higher frequencies, particularly when harmon- frequencies F2 or higher. Sidebands lower than the carrier are ically concordant, suggests suppression of the fundamental, evident intermittently in the adult vocalizations of some which may not constitute the carrier frequency of the individuals of Scotinomys, principally 2nd-generation animals. stereotyped call. As well, there are distinct differences in the lower frequency Function.—The songs of baiomyines are characterized by limits of type I frequency modulation (the song), and type II a number of features that make them ideally suited for
FIG. 12.—Vocalizations of infant baiomyine mice. Two- to 4-day-old pups of Baiomys musculus: A) audible vocalizations and B) ultrasound type II variants. Five-day-old pup of Scotinomys teguina: C) ultrasound type II variants. Seven-day-old pup of CD1 strain of Mus musculus:D) separation ultrasonic vocalization. 1460 JOURNAL OF MAMMALOGY Vol. 88, No. 6 localization. Calls that are frequency modulated and amplitude frequency-modulated ultrasound. Such vocalizations, both modulated in nature serve a role in identifying location, using simple and complex, are known to occur during mating in many cues such as harmonic degradation and attenuation to mark species of murid mice, best known from studies of laboratory changes in position and distance (Bradbury and Verhencamp mice and rats (Bartholemy et al. 2004; Holy and Guo 2005; 1998; Lewis 1983; Peters and Wozencraft 1989). This is Nyby 1983; Nyby and Whitney 1978; Nyby et al. 1979, 1981). particularly true if the animal is at, or near, ground level These vocalizations serve a purpose in courtship, hypothesized (Gerhardt 1998), as is the case with the terrestrial habits of to represent a less-threatening, supplicatory state in males. baiomyine mice. Likewise, maximum localization potential is Invoking allometry in spectral features.—Darwin (1871, achieved when sounds are broadband, repetitive, or ongoing 1872) suggested that there was an inverse relationship between (Lewis 1983; Waser 1977, 1982). Signals of low fundamental pitch and body size, observing that larger animals generally had frequency, although favorably propagated over distance in voices of lower pitch than smaller animals, and likewise forest environments, are quickly absorbed over ground when dominant animals (presumably larger in body size or mass) produced in a terrestrial context (Wiley and Richards 1978). would produce vocalizations of lower pitch than subordinates. Pure tones of narrow bandwidth suffer the least attenuation in These relationships, summarized by Hauser (1997:476), in turn cluttered habitats, such as in leaf litter or herbaceous forest led to ideas regarding the assessment of size, pitch, and edge, allowing signals to propagate more effectively. Con- motivational state of the sender (see for instance Collias 1959; versely, short wavelengths associated with high spectral Morton 1977; Morton and Owings 1998). For example, an frequencies penetrate less easily in a cluttered environment inverse relationship of body size to frequency spread has been and are subject to degradation and distortion. noted within mysticetes and ondontocetes (Matthews et al. The use of lower frequencies (such as those characterizing 1999), rhesus macaques (Fitch 1997), and other nonhuman the calls of Scotinomys) may in part reflect ecological primates (Hauser 1993). Given this, smaller mice should use constraints on sound transmission in leaf litter and cluttered higher frequencies than larger ones, when comparing taxa forest edge habitat typical of Scotinomys, in contrast with the within the baiomyines. However, there are notable exceptions more openly herbaceous and xeric habitats of Baiomys. to the rule (summarized in Hauser 1997), particularly when Likewise, Baiomys is nocturnal and crepuscular (Eshelman mitigated by ongoing selection (Hauser 1993). and Cameron 1987; Packard 1960; Packard and Montgomery Both Baiomys and Scotinomys are tiny mice, with Baiomys 1978), whereas Scotinomys is crepuscular and diurnal (Hooper being smaller on average than Scotinomys. Body mass in B. and Carleton 1976). Habitats providing greater visual pro- taylori ranges from 6 to 9 g (Eshelman and Cameron 1987) and tection may allow foraging and social activity (including vocal B. musculus averages larger (7–9 g—Blair 1941; 8–12 g—Reid communication) to take place during daylight by Scotinomys, 1997), whereas S. teguina ranges from 7 to 13 g and S. relaxing constraints against the use of more persistent and xerampelinus from 9 to 13 g (Reid 1997; see also Hooper and localizable acoustic features. Carleton 1976). Despite significant overlap in mass between B. Localizability entails an immediate risk to the signaler, if the musculus and either species of Scotinomys, the 2 genera are signal falls within the hearing range of either predators or distinguishable in spectral elements. We would expect greater competitors. Payoffs can be manifold, ranging from increased similarity in the frequency range and peak if pitch was a direct vigilance and group safety, to the maintenance of pair contact, function of body size and mass. Given the smaller mass of to locating potential mates. For instance, in the case of B. taylori of the 2 Baiomys species, we would expect the song Richardson’s ground squirrel, an increased ability to localize of B. taylori to have the highest frequencies used by the alarm call elements has been hypothesized to promote Baiomyini. Yet, B. musculus achieves the highest maximum hypervigilance, potentially enhancing safety for conspecifics and peak frequencies during song. Likewise, S. teguina can when in the presence of terrestrial predators (Sloan et al. 2005). equal, or even exceed B. taylori in its upper frequency limit, As such, the production of localizable signals can reflect more despite the smaller average mass of B. taylori. As such, body proximate motivating factors, such as the reliable estimation size in the Baiomyini does not exhibit the expected negative of the location of a threat. correlation with performance frequency. An improved ability to localize also would be important if Behavioral systematics.—Species-specific call structure is calls with such features were co-opted to assume a role in generally termed signal ‘‘identity’’ (Peters and Wozencraft reproductive behavior, or in pair-bond relationships. Both 1989). It is based on the presumption that vocal labels contain genera are known for solicitous social behavior, with evidence stable elements that are uniformly recognized by all con- of parental investment by both sexes to varying degrees (Blair specifics and coincide with taxonomic boundaries. Syntactic 1941; Hooper and Carleton 1976; but see also Packard 1960). traits, found in some territorial songs, likewise correlate with The more elaborate calls of S. teguina and greater propensity for genetic distances among taxonomic units (for instance Packert vocal reciprocity coincide with more extensive nest building, et al. 2003), and their variation can contain phylogenetic and a greater degree of parental investment and cooperation, and phylogeographic signal. Thus, subtle acoustic differences features of life history that suggest a relatively more K-selected among lineages can provide systematic information. reproductive strategy (Hooper and Carleton 1976; sensu Loud long calls and song are taxonomically informative and MacArthur and Wilson 1967). A more proximate role in have been used in a number of phylogenetic analyses (Geiss- reproductive behavior has been hypothesized for the use of man 1993; Haimoff et al. 1982; Strusaker 1970; Zimmerman et December 2007 MILLER AND ENGSTROM—SINGING BAIOMYINE MICE 1461 al. 1988). The subfamily Neotominae (family Cricetidae) itant with similar frequency-modulated elements in the neo- includes 16 genera and approximately 120 species of New natal vocal repertoire. There are few developmental data World mice and rats (Musser and Carleton 2005). Although pertaining to the acoustic behavior of baiomyine species, so it systematic relationships within this subfamily are not fully is unclear whether our limited observations of pups of B. resolved, formal recognition of the tribe Biaomyini is supported musculus and S. teguina can link a juvenile precursor to adult by both morphological and molecular evidence (Bradley et al. song. Whether retained or derived as a behavioral feature, 2004; Carleton 1980; Carleton et al. 1975; Engel et al. 1998; unique song similarities among the Baiomyini underpin its Hooper and Musser 1964; Musser and Carleton 2005; Rogers et cohesion as a clade. al. 2005). We now add behavioral evidence that is likewise synapomorphic, but also taxonomically informative at the ACKNOWLEDGMENTS species level: the steeply modulated, temporally complex and We thank R. Dowler, Department of Biology, Angelo State highly stereotyped songs of Baiomys and Scotinomys. University, San Angelo, Texas, for allowing us to house and record The calls of the 2 genera of baiomyines are of a character a study colony of Baiomys and Onychomys, and for the opportunity to and nature undocumented in other murid taxa. Overall, observe these mice, both in the laboratory and the field. We also thank taxonomic structure is well defined and unambiguous, regard- E. Arellano, D. Valenzuela, and F. Gonzalez, Centro de Educacio´n Ambiental e Investigacio´n Sierra de Huautla, Universidad Autonoma less of sex. However, the degree to which sexes segregate in del Estado de Morelos, for providing laboratory facilities in Morelos, multivariate space is also a unique taxonomic character. The Mexico, and access to field sites, but especially for the hospitality principal component analysis indicates that, in accord with the extended during the many legs of this research. M. Hidalgo, Station univariate data, Scotinomys in general are more dimorphic than Manager, Estacion Biologica Monteverde, Costa Rica, kindly extended Baiomys, with nearly complete separation of males and access to outbuildings and assisted with many logistical issues during females. B. musculus has less pronounced separation of sexes fieldwork in Costa Rica. We thank J. Guevera, El Ministerio Del and, in B. taylori, males and females are randomly interspersed Ambiente y Energia, Sistema Nacional de Areas de Conservacion, (monomorphic). Thus, although both the temporal and spectral Costa Rica, for assistance navigating the logistics involved in elements in the baiomyine call contribute to species identity, obtaining our laboratory colony. D. Valenzuela provided the sample the degree of dimorphism present in them also appears of B. musculus (Mexico), and R. Dowler the samples of B. taylori and taxonomically significant. Onychomys. Work in Texas occurred also under scientific permit No. SPR-0602-224. The Scotinomys sample was obtained under the Costa Investigations among related genera of neotomine rodents Rican Government scientific permits 225-201-OFAU and 047-2002- suggest that repetitive and stereotyped vocal signals are not OFAU, and Area de Conservacio´n Cordillera Volcanı´ca Central y el confined to the baiomyine clade, but have been identified in Programa de Investigacio´nes, Costa Rica (ACCVC), scientific permit Onychomys (Hafner and Hafner 1978), Reithrodontomys (J. R. 2001-ACCVC-028. This study was funded by the Royal Ontario Miller, in litt.), and some species of Peromyscus (Houseknecht Museum Trust Fund (MDE), Connaught Foundation Open Fellowship 1968; Kalcounis-Rueppell et al. 2006; Sales and Pye 1974; also (JRM), and the Ontario Graduate Scholarship Program (JRM). J. R. Miller and M. D. Engstrom, in litt.). 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Pp. 403–431 in Behaviour of marine animals: current males plus 4 additional F2 males (Cartago, Costa Rica, ROM 116802 perspectives in research. Vol. 3. Cetaceans (H. E. Winn and B. L. [21], 116803 [32], 116806 [25], 116807 [33], 116808 [8], 116809 Olla, eds.). Plenum Press, New York. [20], 116815 [20], 116816 [25], 116823 [14], 116833 [31], 116846 THORPE, W. H. 1961. Bird-song. The biology of vocal communication [33], 117151 [20], 117156 [20], 117158 [32], F48793 [41], F48856 and expression in birds. Cambridge University Press, Cambridge, [27]; Allajuela, Costa Rica, ROM 117154 [22]; San Jose´, Costa Rica, United Kingdom. ROM 116831 [25], 116832 [21], 117155 [35], 117157 [48], 117162 WARBURTON, V. L., G. D. SALES, AND S. R. MILLIGAN. 1989. The [34]); and S. xerampelinus, 4 females, 4 males plus 1 additional F2 emission and elucidation of mouse ultrasonic vocalizations and the male (Cartago, Costa Rica, ROM 116810 [43], 116812 [31], 116813 effects of age, sex and gonadal status. Physiology and Behavior [22], 116828 [30], 116829 [31], 117159 [31], 117708 [38], 117709 45:41–47. [18], 117710 [28]). December 2007 MILLER AND ENGSTROM—SINGING BAIOMYINE MICE 1465
APPENDIX II Paired-sample Wilcoxon signed-rank tests of time-expansion versus real-time random data for 15 individual Scotinomys. Assumptions of normal distribution were not met for variables total duration and number of notes; however, paired-sample t-tests (d.f. ¼ 14) are relatively robust against such violations and we include this test statistic as a more conservative assessment of instrumentation bias. The t-statistic and significance (P) are given in parentheses.
Variable Wilcoxon Z (t-statistic) Asymptotic significance (P) Total duration 0.398 ( 0.565) 0.691 (0.581) Number of notes 0.398 (0.159) 0.691 (0.876) Minimum frequency 1.591 ( 1.954) 0.112 (0.071) Maximum frequency 0.284 ( 0.339) 0.776 (0.740) Peak frequency 0.511 ( 0.633) 0.609 (0.537) Bandwidth 1.306 (0.713) 0.191 (0.488)